J. theor. Biol.

(1976) 56, 95-110

The Retrieval of Learned Information--a Neurophysiologieal

Convergence-Divergence Theory
J. GRINBERG-ZYLBERBAUMt

Brain Research Laboratories, New York Medical College,

106th Street and Fifth Avenue, New York, N.Y. 10029, U.S.A.

(Received 21 May 1974, and in revisedform 20 December 1974)

The information in the brain is associated with specific patterns of electrical
activity, resulting from the firing characteristics of neurons and circuits
located in a tridimentional complex space. The external world is represented
in this space after an energy transformation. From this representation,
common features are extracted by way of convergent circuits. These
circuits concentrate in few neuronal elements information that prior to
their activation is distributed in a great deal of neurons. The convergence
circuits are arranged in a hierarchical order in which each one of them
receives information from the previous.
In each hierarchical level of convergence, more abstract and con-
centrated characteristics of the information is handled. At some levels,
the convergence circuits from various sensory modalities interact by way
of polisensory neurons. Thus, language and complex associations are
derived from them. The retrieval of stored information involves the acti-
vation of these high convergence polisensory circuits that in turn stimulate
divergence circuits that duplicate similar patterns of neuronal activity as
the ones activated when the now retrieved information was perceived.

1. Introduction
Each object that is perceived is transformed in the retina in a complex but
specific spacio-temporal pattern of neuronal activation. This complex
pattern contains all the information a b o u t the object.
The subjective perception takes place when the complex pattern o f neuronal
activation arrives to the cerebral structures in which the analysis a n d de-
codification o f the pattern is done.
The retrieval and evocation o f the stored information a b o u t the object
arises when some parts or perhaps all the pattern activated, is duplicated by
way o f some stimulus that triggers it. In this sense, the perceptual process is
inseparable from the complex retrieval process. Experimental evidence in
I" Present address: Prisciliano Rodrtguez 20 Tepoztlan Morelos, M6xico.
95
96 J. GRINBERG-ZYL]3ERBAUM

accord to this postulation was first obtained in a study made by Livanov &
Poliakov (1945) in which the so-called "assimilation of the rhythm" phen-
omenon was described. Following a classical conditioning association
procedure, a cortcial EEG rhythm of 3 c.p.s, began to appear when a con-
ditioned stimulus was applied, and later on was observed even during the
intertrial intervals. These facts seem to point towards the interpretation that
the frequency of the electrical rhythm contained the information about the
stimulus. Furthermore, Yoshii, Prover & Gastaut (1957) found that the
assimilation of the rhythm phenomenon was aroused when an animal was
placed in the site in which it was conditioned but it did not arise in a non
associated place. This finding means that the electrical activity that represents
information can be triggered and retrieved by parts of the stimuli complex
present during the acquisition of the learning paradigm. The fact that the
same rhythm appeared during the real presentation of the stimulus and in
its absence, but in the presence of part of the stereotype that was asso-
ciated with it, indicates that the brain acquires a representation of the stim-
ulus complex, that corresponds with the particular electrical activity that is
released during the retrieval.
In more recent work, John's research group has presented evidence
(Chow, Dement & John, 1957; John 1967, 1972; John, Bartlett, Shimokochi
& Kleinman, 1973; John & Killam, 1959, 1960; John, Leiman & Sachs,
1961; John, Ruchkin & Villegas, 1964) that extends the latter findings.
In one of their earliest approaches (John & Killam, 1959), they conditioned
cats~to avoid an electrical shock by responding to a flickering light of 10 c.p.s.
When this light attained a cue value, it was observed that the electrical activity
of the visual cortex and other structures began to correspond to the frequency
of the light. Later on when another frequency of the flickering light was
introduced and the animal made a generalized response to it manifesting the
same avoidance behavior, the electrical activity corresponded to the inter-
prctation (informational content) that the animal gave to the stimulis and
not to its physical characteristics. That is to say, the electrical activity was
the same as the one recorded when the stimulus was actually of 10 c.p.s.
When the animal began to differentiate the new light by not responding to it,
the electrical activity began to correspond to the physical characteristics of
the now differentiated stimulus. This means, that the actual informational
value of one stimulus is related to its capacity to evoke stored information,
and this in turn is well correlated with the patterns of electrical activity
that are evoked by it. The informational value of the electrical rhythms seems
to be independent of the particular learning paradigm used. This fact was
demonstrated in a study by John & Killam (1960) in which animals were
conditioned to press a lever in response to a stimulus of 10 c.p.s, and not
 RETRIEVAL OF I N F O R M A T I O N IN THE BRAIN 97

press it when it was of 6 c.p.s. In the initial presentations of the 6 c.p.s.

stimulus, when the animals responded to it as if it were of 10 c.p.s., the
electrical activity of the cortex, lateral geniculate, reticular formation,
hippocampus and fornix corresponded to the one recorded when the 10 c.p.s.
stimulus was actually presented. This means that the real informational value
of a stimulus complex is not associated with its physical characteristics,
but instead with its capacity to release a previously stored representation,
manifested in a particular and specific electrical rhythmical activity. The
behavioral interpretation that one animal makes about a stimulus represents
the particular form in which the stimulus is integrated and perceived. The
correlation between the representation and the electrical activity that is
associated with it indicate the important informational content of this
activity. On the other hand, the studies above mentioned indicate that the
perception processes are inseparable from the retrieval processes associated
with stored information. Only this interdependence explains why the same
physical stimulus results in different behavioral outcomes.
The idea that the codified information about an external stimulus is
related to particular patterns of electrical response is also supported by the
studies of Colavita (1973) in which an external conditioned stimulus of
specific frequency that has been utilized as a conditioned one, is substituted
by direct electrical stimulation of the brain at the same frequency. This
direct stimulation evoked exactly the same response as the one obtained
with the external stimulus. Furthermore, if the behavioral paradigm implies
responding in two different forms to two distinct external stimuli that
differ in frequency, the direct stimulation with the two frequencies result in
the two behavioral responses, each one controlled by the internal frequency
in the same way and specificity as the two external ones.
The pattern of electrical activity that is aroused when a stimulus acquires
informational value does not depend upon the physical characteristics of
the stimulus, but instead upon the way that it is interpreted. This "inter-
pretation" in neurophysiological terms must involve some mechanism that
transforms the incoming signal in the pattern of neuronal activity that
corresponds to the stimulus complex with which it has been associated. The
incoming signal establishes some interaction with a stored pattern. This
latter pattern is the one that appears and not the one that corresponds to
the physical characteristics of the external stimulus.
Herrington & Schneidau (1968), studying humans, found that the visually
evoked responses differed in wave shape depending if the stimulus that
arouse them was a circle or a square equated in area. If the subject was
later asked to imagine a square or a circle each time a flash illuminated a
blank field, clear reproducible differences in wave form were produced to
T.B. 7
98 J. G R I N B E R G - Z Y L B E R B A U M

each of the imagined figures and they resembled the waveforms obtained
with the actual stimulus. This ingenious study indicates that the real percep-
tion and the imagined one (that is the retrieved one) are accompanied and
related to the same type of electrical activity.
If the electrical rhythmical activity and the waveform of the evoked poten-
tials are so nicely correlated with the informational content of a stimulus,
we can expect the unitary activity from which the latters result (Fox &
O'Brien, 1965; Morrell, 1967) to manifest similar relations. Perhaps the most
clear and thoughtful study in this respect is the well known research done
by Morrell (1967). In the first stage of his study, Morrell recorded the activity
of single cells in the visual cortex (visual area III) of the cat during the appli-
cation of visual, acoustic and tactil stimuli. A great majority of the cells
studied were polisensory in the sense that they responded to different
modalities of stimulation but they manifested particular response patterns
that were specific and different depending on the stimulus used. The response
patterns differed even for stimuli of one modality but with different character-
istics. Thus a vertical bar with a length of 3.6 cm moving from left to right
in a dark room gave a different response pattern from the one obtained from
the same stimulus but moving in the opposite direction. Once the above
facts were determined and the specific response patterns of the cells responding
to different stimuli were recorded, the author began to stimulate his animals
with combinations of stimuli.
The cells response to the combined stimuli had extremely complex patterns
that in some cases resembled a simple linear summation of the firing patterns
for each separate stimulus, although the majority of the cases were more
complicated than the ones expected to arise from a simple sum. The com-
bined or associated presentation of the stimuli were usually repeated until
two blocks of 20 trials each were given. Following this procedure, the "pre-
ferred" stimulus of the pair was presented alone. In approximately 10~o of
the cells studied, the single presentation of this stimulus evoked stable res-
ponse patterns with a marked resemblance to those elaborated by the
combined stimuli. If the presentation of the single stimulus was continued
without being associated with the other member of the pair, the response
pattern began to resemble the one obtained prior to the association maneuver.
But if the combined presentation was now reinstalled, very few trials were
necessary to achieve the transformation in the response pattern. These facts
indicate that the firing pattern of a neuron can be changed by an association
procedure. Furthermore, the changes obtained resemble the response aroused
during the combined or associated presentation. Thus the patterns of neuronal
activity represent the end product of stored experiences and are not the
result of the unchangeable and direct physical characteristics of the stimulus.
 RETRIEVAL OF INFORMATION IN THE BRAIN 99
A very interesting fact arising from this same study is that the cells that
displayed the capacity of combining and storing the associated pattern were
only those with a polimodaI character, that is the ones that responded
previously to any manipulation to the stimuli that were later on associated.
John (I972) discusses this fact as evidence that suggests that the crucial
event in learning is not the establishment of new connections between cells
but the enacting of a new pattern of activity in the already existing connec-
tions. This postulation is in accordance to the findings of Hubel & Wiesel
(1963) and Wiesel & Hubel (1963, 1965) about the fact that in very young
visually inexperienced kittens, the cells of the visual cortex respond in a
normal fashion to complex visual stimuli, as if the neuronal circuits asso-
ciated with these responses existed prior to birth, but if the cat does not
use these circuits, they begin to deteriorate.

2. The Retrieval of Stored Information in the Nervous System

There are different types of retrievals of stored information. One of them
is the phenomenon associated with saving in relearning. A second type
involves the simple recognition of one stimulus complex. A third type occurs
when the name of an object is evoked when this object is visually perceived
or on the contrary, when the verbal information about an object arises an
image of it. Finally, there is a redintegrative type of retrieval in which a
complete reconstruction of some past experience is achieved. All of them
arise as a consequence of the presentation of a previously associated stimulus
that now triggers the activation of a memory store. If the information in the
nervous system is represented as specific neuronal patterns of activation,
then the stimulus that trigger's the retrieval must be capable of arousing them.
The specific type of retrieval probably depends upon the capacity of the
trigger stimulus to duplicate the exact pattern in a more or less complete
form. Two questions must be answered before we continue: firstly, how does
the trigger stimulus become capable of causing the retrieval ?; that is, the
pattern. Secondly, on what does the exact duplication of it depend? To
answer the first question, we must make an analysis of the characteristics
of some sensory system, hoping that this analysis will help in arriving at
some conclusion that could answer the question. The second problem will
be treated later on.
There are at least four different types of cells in the visual cortex of the
cat (Eysel & Grusser, 1971 ; Hubel & Wiesel, 1965). The first type is known
as simple. They are found mostly in the visual area 17 primary visual cortex
(Hubel & Wiesel, 1965). Their fields are concentric (as the ones found in
contrast cells in the lateral geniculate body) or elongated (Hubel & Wiesel,
100 J. GRINBERG-ZYLBERBAUM

1962, 1965). The position of the stimulus in the retina is very critical for these
neurons. The orientation of the stimulus that evokes an optimal response in
these ceils is also critical (Hubel & Wiesel, 1962). In the same area 17 and in
the adjacent 18 (secondary visual cortex) there are complex cells. These units
respond in a similar way as the simple cells do, but their fields are longer
in size and never concentric in form (Eysel & Grusser, 1971 ; Hubel & Wiesel,
1962, 1965). The response of these cells is independent of the part of the
field stimulated. It is very probable that the complex cells receive convergent
information from simple cells; at least, this is the best explanation of the
similarity of response and the increase in the size of the receptive fields.
The third type of cells are the low order hypercomplex units, found in
areas 18 and 19 (tertiary visual cortex). They respond, as do complex cells,
to a slit and edge or a dark bar, but the length of the stimulus is critical.
The optimal stimulus is thus a critically oriented line falling within a given
region of the retina. Similar stimulus in adjacent portion are inhibitory to it
(Hubel & Wiesel, 1965). The responses of these cells are explained by assum-
ing convergent circuits arising from complex cells, some being facilitatory
and some inhibitory. The fourth type of cells are the high order hypercomplex
units. Their responses resemble the ones found in lower order hypercomplex
cells, but differ when responding to the line in either of two orientations, 90°
apart (Hubel & Wiesel, 1965). They are found mostly in tertiary cortex and
as the lower order cells; they respond optimally to directionally moving
stimuli. The size of the receptive fields of the higher order ceils is much
longer than the one found in lower order units and their response does not
vary in respect to the part of the field stimulated (Eysel & Grusser, 1971).
In general, the behavior of the higher order cells is as though they receive
their input from a large number of lower order hypercomplex cells (Hubel &
Wiesel, 1965). The independence of response in these cells in relation to the
localization, of the stimulus in their receptive fields means that these neurons
are not influenced by localization. This fact can be explained by the
assumption that neurons that respond to a complex stimulus, converge in
them.
The organization of the cat's visual cortex is columnar. Each vertical
column contains similar cells in relation to their complexity, best orientation
of the stimuli, etc. (Hubel & Wiesel, 1962, 1965). Similar findings have been
reported in the monkey (Hubel & Wiesel, 1968; Wurtz, 1969). The field size
of the complex cells in these animals is larger than that of the simple units
and smaller than that of the hypercomplex cells (Hubel & Wiesel, 1968).
It is supposed (Hubel & Wiesel, 1968) that the simple cells receive con-
vergent information from concentric cells in the lateral geniculate body. The
complex ones receive convergent information from the simple cells. The
 RETRIEVAL OF INFORMATION IN THE BRAIN 101
lower order hypercomplex cells receive convergent information from complex
cells and the high order hypercomplex ceils receive convergent information
from lower order hypercomplex cells (Hubel & Wiesel, 1968). These high
convergence circuits explain the increase in complexity from simple to high
order hypercomplex cells and the increase in receptive field size. In informa-
tional terms, this increase of convergence means that very complex informa-
tion is concentrated in fewer channels as we move from the periphery to
the central portions of the system. In this sense, relatively few cells contain
the same information that was previously related to the activity of a much
greater number of elements. This "concentration" of information is perhaps
done at the expense of complicating the neuronal pattern of response in the
high convergence units.
The visual information does not remain and stop at the level of the tertiary
visual cortex, there is evidence that indicates that the visual cortex projects
itself onto other structures (Curnod, Casey & McLean, 1965; Chalupa,
Harvey & Lindsley, 1972; Dow & Dubner, 1969; Gross, Rocha-Miranda &
Bender, 1972; Hubel & Wiesel, 1969; Kass, Hall & Diamond, 1972; Pribram,
1972); this evidence also shows that the response of the cells in some of these
structures can be more complicated (in terms of the optimal stimulus that
makes them respond) than the ones recorded in area 19 (Gross et al., 1972).
For example, it has been found in monkeys that some cells of the infero-
temporal cortex respond in an optimal way to the presentation of a visual
pattern that resembles a monkey's hand (Gross et al.,1972). This evidence
indicates that perhaps the convergence circuits are maintained and exagger-
ated at this level. This means that the information is more concentrated in
these structures and it contains the information associated with the activity
of the previous ones. Other structures in which the concentration of informa-
tion may take place are the pulvinar nucleus and the caudate nucleus (Buck-
wald, Rakic, Wyers, Hull & Heuser, 1962; Chalupa et aL, 1972; Grinberg-
Zylberbaum, Carranza, Cepeda, Vale & Steinberg, 1974; Grinberg-Zylber-
baum et al., 1973; Kaas et aL, 1972; Pribram, 1972). Similar processes seem
to be associated with the auditory system. In this system, it was found
(Evans, 1971) that in the peripheral structures, the cells respond to relatively
simple sounds (i.e. pure tones), while the responses of the cells in the auditory
cortex are associated to much more complex sounds. These are units that
respond in optimal form to a sound that varies its frequency in a sequential
form. The optimal sequential variation occurs in the sense of increasing,
and/or decreasing, the pitch. These types of responses can only be explained
if these ceils receive convergent information from cells that respond to each
of the frequencies of the complex sound. Furthermore, the fact that they
respond specifically to an increase or to a decrease in the sequence of
102 J. GRINBERG-ZYLBERBAUM

frequency, is explained by assuming the existence of lateral inhibitory circuits

that become activated only when the activation of the cells is in some pre-
ferred sequence. Here again, as we move away from the peripheral portion of
this system, there is an increase in convergence that makes the reduction in
the number of channels that convey complex information possible. The
auditory information (as the visual one) probably does not remain in the
auditory cortex. There is evidence about the existence of extra auditory-
cortical areas that respond to sound stimuli (Albe-Fessard, Oswaldo-Cruz
& Rocha-Miranda, 1960; Albe-Fessard, Rocha-Miranda & Oswaldo-Cruz,
1960; Bental & Bihari, 1963; Grinberg-Zylberbaum et al., 1973; Sedwick &
Williams, 1967; Thompson, Johnson & Hoopes,1963; Thompson, Smith &
Bliss, 1963). Perhaps some of them receive very complex and previously
integrated auditory convergent information.
If as stated before, both the visual and the auditory systems have as a
characteristic the increase of convergence, and if the convergence circuits
of the two systems establish a mutual communication at some level in the
nervous system, then a functional interaction between them becomes possible.
The communication is probably made with polimodal-polisensory units in
which the association of patterns can be achieved. The existence of poli-
sensory neurons and of common brain areas of interaction between the
auditory and visual modalities is a well known fact in actual neurophysiology.
Cerebral structures such as the pulvinar nucleus (Allman, Kaas, Lane &
Miezin, 1972; Chalupa et al., 1972; Wright, 1971), inferotemporal cortex
(Gross et al., 1972; Pribram, 1972), caudate nucleus (Albe-Fessard et aL,
1960a, b; Encabo & Buser, 1964; Grinberg-Zylberbaum et al., 1973; Schiller
& Stryker, 1972), reticular formation (Hernandez-Peon, 1955, 1961; Yoshii
et al., 1957), "association cortex" (Bental & Bihari, 1963; Thompson et al.,
1963a, b) and even the visual cortex (MorretI, 1967; Murata, Cramer & Bach
y Rita, 1965) fulfil the latter characteristics. Furthermore, if the polisensory
neurons are of the same class and capabilities as those described by Morrell
(1967) then not only an association between patterns becomes possible but
also a triggered duplication of them. This postulation may be better under-
stood in the following example. Imagine a man that has never seen a flower.
The first time that we show him a rose, he certainly is able to see it although he
does not know what it is and what it is called. The vision of the rose resulted
from the complex and specific activity of the man's visual system, at least
from the activity of the simple, complex and hypereomplex neurons in the
cortex. At the same time that we present the rose, we give him verbal in-
formation... "This is a flower." If the verbal pattern "flower" is pronounced
each time that our hypothetical man sees the rose, there will be a moment
in which it will be enough to present the visual information (in the absense of
 R E T R I E V A L OF I N F O R M A T I O N I N THE B R A I N 103

the verbal one) for the man to s a y . . . "this is a flower". By the same token,
it will be enough to present the verbal information (in the absence of the
visual one) for the man to imagine a rose. In this case, the image of the rose
is the retrieved visual memory of the previously perceived flower and the
verbal pattern is only the stimulus that triggers and arouses this memory.
In the previous case, the verbalization ("This is a flower") is the retrieved
verbal memory of the previously heard name, and the visual object is only
the stimulus that triggers and arouses this memory. In order to have the
visual or the verbal evocation of the flower, it is necessary to reproduce the
same or similar neuronal patterns of activation that normally occur when
we give the verbal or the visual information. In this particular case, the
neurons of the primary, secondary and tertiary visual cortex, or the corres-
ponding cells in the auditory one must become activated with similar
electrophysiological patterns to the ones corresponding with a real per-
ception. If this is true, then definitely the neuronal verbal flower pattern
must be enough to give place to the visual rose and/or the neuronal visual
rose pattern must be enough to give place to the verbal one. The real presenta-
tion of a flower activates millions of receptors at the retinal level. This
activation converges into the axons of the optic nerve and after passing
through the lateral geniculate body, arrives to the primary visual cortex
where a great number of simple type cells begin to respond. The activation
of these cells converge into the complex ones and their activity activates the
convergent circuits that are connected with the hypercomplex neurons.
From here the highly concentrated visual information travels to high
convergence polisensory neurons that at the same time receive highly con-
centrated verbal patterns. The cells so activated respond with a complex
pattern that is a sort of combination of both and because of this, contains
them.
By a process previously unknown, these cells can store the combined
pattern and respond to each one of the single stimulus with it (Morrell,
1967). This does not mean that memory is contained in a private form in
some neurons; I think that these units participate in a lot of evocation pro-
cesses; the specific memory that is evoked is probably dependent upon the
specific pattern of activation that arrives to them and triggers their response.
The activation of the polisensory neurons and the display of the highly
concentrated information contained in their pattern of response, is perhaps
the first step in the process of retrieval and evocation of stored information.
If the retrieval process stops at this level, surely neither visual image nor a
verbal manifestation is obtained. For these to take place a more complete
and duplicated activation of the patterns must take place.
We now face a most delicate and difficult problem that was already
104 J. GRINBERG-ZYLBERBAUM

mentioned in a previous section: how is the exact duplication of the cerebral

cortex patterns achieved? First of all, the previously postulated existence of
high convergence polimodal cells in which the association between patterns
takes place, has a logical and theoretical value. The association processes
are much easier, exact and economical in a system of relatively few elements
that contain very complex and concentrated information, than in one that
contains a giant number of cells in which the information is dispersed and
fractioned between the elements that constitute it. At the same time, the most
logical way to explain how the duplication of the patterns in the cerebral
cortex is achieved as a result of the polimodal cells responses, is by postulating
the existence of divergence circuits from those neurons to the cells of the
cerebral cortex. If this hypothesis is true, then the hypothetical divergence
circuits to the cortex must be activated in a specific form when a particular
combined pattern of activation arises in the high convergence polimodal
cells. Perhaps the rhythm, frequency and other characteristics of the patterns
in these neurons are able to "open" and make respond specific divergence
circuits. This "opening" could be related to the specific refractory periods or
the capacity to follow certain frequencies in the neurons conforming the
divergence circuits, so a change in the codification of the polisensory neurons
could be the critical factor that determines which divergence circuits become
active and which characteristic patterns of responses arise in them. All the ideas
mentioned could explain why, when someone tells us to have an image about
a flower we can see a rose and why when we see a rose we can mention the word
flower. Obviously, the word flower can stimulate the image of a lot of
different flowers or parts of them so that the image is very rarely complete
and clear.
This means that the accurate and total reproduction of the visual stored
pattern is very difficult to achieve, being the activation of only some parts
of the patterns the most common, probably those parts that are common
to all the flowers. The accurate and total reproduction of the visual or other
modality stored patterns and the specific type of retrieval (see the section
about types of retrievals) achieved, probably depends on the fulfilment,
more or less, of at least the following conditions:
(1) the exact duplication of the pattern in the polisensory neurons;
(2) the same state of excitability of the divergence polimodal-cortex
circuits during the acquisition and during the retrieval of perceptual in-
formation;
(3) the complexity of the stored information.
The last point is understandable because it is easier to evoke the word
flower when we see a rose than to imagine a rose when we hear the verbal-
 RETRIEVAL OF I N F O R M A T I O N IN THE BRAIN 105
ization; perhaps this fact is related to the different quantity of divergence
circuits that must be activated in the visual or the auditory systems. The
necessary duplication of the state of excitability in order to have the repro-
duction of the patterns and so the retrieval of information is very well illus-
trated in the so-called state dependent learning experiments, where an animal
executes a learned response only if he is submitted during the evocation
session to the same conditions that occurred during the acquisition one
(i.e. drugged state). On the other hand, there must be some logic in the
activation of the patterns; this logic is perhaps related to the number of
stimuli associated or combined. I think that the memory of one event is this
logic of activation and it is not located either in the cerebral cortex or the
polimodal structures but has to do rather with the specific patterns in all the
systems. In this sense, the polimodal neurons are prepared to respond with
a combination of patterns when one member of the association is presented;
this would be the readout of memory. The combined pattern in turn and by
way of divergence circuits, activates the structures that normally are involved
in the "perception" of stimuli: these would be the evocation processes, and
all together constitute the memory of one event. One process that is difficult
to explain in this hypothetical model, is the characteristics of the divergence
circuits. One possibility is that the divergence circuits are in some way the
same but inverted as the convergence ones. This means that the activation
can be initiated in the polisensory cells. From here the high order hyper-
complex neurons are activated; later the low order hypercomplex ones,
and finally the complex and the simple cells are also activated. If the portions
of the cerebral cortex so activated are related to its columnar organization
(Hubel & Wiesel, 1965) and each column is associated to a particular feature
of the stimulus, then the quantity and the specific spacio-temporal organiza-
tion of the columnar activation gives the appearance of a particular evoked
image. Each column in its activation represents the "perceptual units"
from which a complex image is constructed. The specific activation of a
mosaic of columns may be the basic and fundamental process of perceptual
and retrieved reconstruction of the external world. Depending upon the
state of excitability of the divergence circuits, one or another image would be
retrieved and so different memories would be evoked. Only if the state of
the system remains the same as the one existing in the original activation
during the perception phenomenon then the information that is evoked is
the same. Another possibility is that the activation of the cerebral cortex
as a result of the activity of the polimodal cells is by means of some inter-
mediary structure. In the visual system this structure could be either the
superior colliculus, the pulvinar, the inferotemporal cortex or the lateral
geniculate body and from here using the normal pathways, the visual cortex.
106 J. GRINBERG-ZYLBERBAUM

The recent finding of John et al. (1973) about the clear and replicable
appearance of the readout potential in the lateral geniculate body is perhaps
a manifestation of the above processes; The emphasis placed in the cerebral
cortex as the structure that needs to be activated in order to have a complete
retrieval of stored visual information is based on the experiment of Herring-
ton & Schneidan (1968) (see the evoked potentials section in this paper).
Here, a duplication of the morphology of a scalp recorded evoked potentials
(most probably arising from the cerebral cortex) was found when a geo-
metrical figure was actually presented or an imagined retrieved one was
suggested, and also the fact that the lesion in the visual cortex produces a
blind condition in humans. Obviously, this evidence is not enough to validate
the above idea. Research on the capacity to retrieve visual information in
human beings who have been recently lesioned in the visual cortex is one
way in which this hypothesis can be proved. On the other hand, the idea
that polimodal cells contain and participate in the codification of visual
information, and that their activity is necessary in order to activate the
retrieval of stored information is now under experimental study in several
laboratories. In a recent experiment (Grinberg-Zylberbaum et al., 1974)
the electrical activity of the caudate nucleus of rats was disorganized by
applying single square electrical pulses, while these animals were watching
other rats pressing a lever in a Skinner box. The stimulation of this poli-
sensory structure impaired this learning by observation. This study indicates
the important participation of this structure in the integration of visual
information.
The retrieval of stored information is never a static enterprise, when we
remember the image of an object as a result of a verbal order, we do not see
a stable photograph of it, but instead a sequence of internal dynamic visions
that have movement. This movement and dynamics seems to be independent
but triggered by the verbal pattern. The independency is in the sense that
the verbalization, in the majority of cases, does not have the explicit sequence
in spite of the obvious fact that the image does. In the same way, when we
remember the name of an object while we see it, the verbalization is a sequence
of specific sounds in a particular order. If as stated before the activity of the
polimodal cells is the beginning of the retrieval process, this activity must
change and contain the appropriate sequence. The neuronal processes
responsible for the retrieved sequence are unknown but perhaps they arise as
a result of a memory sequenciator that stores them in separate depots that
interact and trigger the activity of the high convergence polimodal cells.
Perhaps this hypothetical sequenciator is related to eye movements. In this
respect and concerning the visual recognition processes, Noton & Stark (1971)
have postulated the following hypothesis: "The internal representation or
 R E T R I E V A L OF I N F O R M A T I O N IN THE B R A I N 107
memory of an object is a piece meal affair: it is an assemblage of features or,
more strictly, of memory traces of features. During recognition (we could add:
retrieval) the internal representation is matched serially with the object, feature
by feature. The features of an object are the parts of it (such as the angles and
curves of line drawings) that field the most information. The memory traces
that record the features are assembled into the complete internal representa-
tion by being connected with other memory traces that record the shifts of
attention required to pass from feature to feature, either with eye movements
or with internal shifts of attention; the attention shifts connect the features
in an order of preference forming a feature r i n g . . . " It can be proposed that
the presentation of verbal information that triggers a visual retrieval, simul-
taneously activates the high convergence polimodal cells and the sequen-
ciator memory store whose activity determines the sequence of combined
patterns of response in the polisensorial neurons. One cerebral structure
whose activity is probably related to the above processes is the superior
colliculus, because of its relationship with the eye movement regulation
(Wurtz & Goldberg, 1972a,b) with the attention phenomenon (Goldberg
& Wurtz, 1972) and its anatomical connections with the retina and the cere-
bral cortex (Michael, 1972).
Finally, the existence of convergence circuits points toward a hierarchical
organization of the brain in which each stage of convergence extracts common
features of information. This extraction is plausible if we think that a
neuron that receives signals from other neurons, responds with enhanced
probability when a coincidence (spatial and temporal) of discharges arrives
to it. In this sense, each level of the hierarchy handles more "abstract"
information by concentrating in a single pattern of response the information
that in previous levels is more "dispersed. It is possible to conclude that at
some level of the convergence hierarchy, language and concept formation
develops. Recently the first evidence of meaning extraction in the brain were
experimentally obtained (Johnston & Chesney, 1974; Grinberg-Zylberbaum
& John, 1974). In these experiments, it was found that the frontal, and
temporal parietal human cortices extract language and conceptual meaning
from the occipital representation of the visual world.

3. Related Phenomena
(A) DUPLICATION OF INFORMATIOH IN THE VISUAL SYSTEM
The visual system has an enormous capacity for functional recovery
after a partial lesion. This recovery is perhaps related to the duplication of
information associated with the divergence circuits that exist from the
108 J. GRINBERG-ZYLBERBAUM
geniculate body to the occipital cortex (Chow, Blum & Blum, 1950). In the
same way, the finding that a 98 ~o lesion of the optic nerve does not impair
complex visual discrimination behavior in cats (Norton, Frommer & Gal-
ambos, 1966), means that the channels that carry visual information have
their duplicity as a distinctive characteristic. This fact is in accord with the
idea that the basic mechanism or process that represents information in the
nervous system is not the activation of specific units but the appearance of
a neuronal pattern of activation.

(13) VISUAL AND AUDITORY RETRIEVAL OF INFORMATION DURING

PARADOXICAL SLEEP
The appearance of visual images and auditory information during para-
doxical sleep is one of the most remarkable characteristics of this stage of the
sleep-wakefulness cycle.
This appearance is perhaps related to the activation of stored electrical
patterns in the auditory and visual cortices.The facility of these patterns to
appear during this stage is perhaps a result of an increase of excitability
in the divergence circuits related to the retrieval of information. This increase
in excitability can be the same one that causes an increase in the magnitude
of the thalamo-cortical potentials (Jouvet, 1967) and in the frequency of
the spontaneous unitary activity during the same sleep stage (Jacobs,
McGinty & Harper, 1973). Furthermore, artificial increments in the number
of paradoxical stage periods have been observed as a result of the lesion of
the caudate nucleus in rats (Corsi, Grinberg-Zylberbaum & Arditti, 1975).
This fact is in accordance with the above interpretation, because of the
evidence that shows that this structure has a normal inhibitory influence on
the excitability of thalamo-cortical circuits (Demetrescu, Demetrescu &
Iosif, 1965; Demetrescu, 1967; Heuser, Buchwald & Wyers, 1961). Perhaps
the same or similar increments in excitability as a result of decrements in
inhibitory network activity explain the appearance of visual and auditory
illusions and even hallucinations in some "pathological" conditions as
schizophrenia.

(C) CONTROL OF COMPLEX MOVEMENTS

Certain complex patterns of movement are entirely programmed at the
level of the spinal cord (Burke, 1973, personal communication). The cortical-
subcortical system related to motor activity seems to send "orders" by way
of the efferent system, that activate the spinal cord circuits related to them.
Probably these "orders" are complex patterns of activation that are recog-
nized by high convergence neurons that in turn activate specific motoneurons
by means of divergence circuits. If this is true, then the motor activity can
 RETRIEVAL OF INFORMATION IN THE BRAIN 109
be interpreted as a result o f a specific process o f retrieval of stored informa-
tion. This situation is very similar to the postulation where the specific
response of high convergence polimodal neurons with a complex pattern of
activation, by means of divergence circuits, activate units in the visual or
auditory cortices and so an image or a complex sound is retrieved.
In fact, there is no logical reason to doubt that the activity of the nervous
system is related to similar processes in all o f the structures and networks
of which it is composed. The apparent dissimilar outcomes of its action
are only related to the different characteristics of the effector organs but not
to the nervous processes from which the activity of the latter results.

This work was supported by the Mexican Science and Technology Council,
CONACYT.

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